Host relatedness and landscape connectivity shape pathogen spread in the puma, a large secretive carnivore

Nicholas M Fountain-Jones,Scott Carver,Ken Logan,Roderick B Gagne,Simon Dellicour,Patricia E Salerno,Mathew Alldredge,Holly B Ernest,W Chris Funk,Meggan E Craft,Daryl R Trumbo,Sue Vandewoude,Kevin Crooks,Roman Biek,Simona Kraberger,Guy Baele

doi:10.1038/s42003-020-01548-2

Abstract

Urban expansion can fundamentally alter wildlife movement and gene flow, but how urbanization alters pathogen spread is poorly understood. Here, we combine high resolution host and viral genomic data with landscape variables to examine the context of viral spread in puma (Puma concolor) from two contrasting regions: one bounded by the wildland urban interface (WUI) and one unbounded with minimal anthropogenic development (UB). We found landscape variables and host gene flow explained significant amounts of variation of feline immunodeficiency virus (FIV) spread in the WUI, but not in the unbounded region. The most important predictors of viral spread also differed; host spatial proximity, host relatedness, and mountain ranges played a role in FIV spread in the WUI, whereas roads might have facilitated viral spread in the unbounded region. Our research demonstrates how anthropogenic landscapes can alter pathogen spread, providing a more nuanced understanding of host-pathogen relationships to inform disease ecology in free-ranging species.

Highlights

Urban expansion can fundamentally alter wildlife movement and gene flow, but how urbanization alters pathogen spread is poorly understood
We found distinct demographic histories in the viruses circulating in the wildland urban interface (WUI) and UB regions, and differing FIVpco subtypes
Bayesian time-scaled phylogenetic analysis of the FIVpco sequences revealed two co-circulating FIVpco subtypes: FIVpco CO, circulating among pumas in both regions (Fig. 1a) and FIVpco WY, which was only detected in the UB after having been previously detected in puma in Wyoming (Fig. 1b; see Fig. S1 for a maximum-likelihood tree that illustrates the broader phylogenetic context of these two subtypes across North America)

Summary

Introduction

Urban expansion can fundamentally alter wildlife movement and gene flow, but how urbanization alters pathogen spread is poorly understood. As urban development fragments habitats and introduces barriers (the wildland–urban interface, WUI), it can cause reduced host gene flow between populations[10,14], altered animal behaviour (for example, animals becoming more nocturnal to avoid humans15,16), and changes in feeding[17] and movement[18] patterns If these anthropogenic impacts on host behaviour affect transmission dynamics, they may manifest in the demographics of pathogen populations[19] (e.g., if transmission events are happening rapidly, the pathogen’s effective population size may be exponentially increasing[19]). We examine what factors impact FIVpco spread using a novel pipeline synthesizing phylodynamic, phylogeographic and landscape genetic techniques (an ecophylogenetic approach[33]) We employ this pipeline to test for (1) differences in FIVpco demographic histories and transmission dynamics across regions, (2) concordant patterns of host relatedness, viral phylogenetics and spatial distance, and (3) the relative roles of host relatedness and landscape predictors, such as urban development, in shaping the pattern of spread of the virus. We hypothesized that as anthropogenic factors impact puma movement (e.g., ref. 34) and gene flow[26] at the WUI, that transmission opportunities would be restricted and spatial proximity and host relatedness would be more important in shaping spread in this region

Methods

Results

Conclusion